Biogenic amine–producing Enterococcus spp. from anchovy (Engraulis encrasicolus): Isolation and molecular insights
Main Article Content
Keywords
Enterococcus; fresh anchovy; biogenic amine; food safety; molecular characterization
Abstract
Biogenic amines (BAs) constitute an important chemical hazard in fish and fishery products, primarily due to their adverse effects on human health. While histamine-producing bacteria have been extensively investigated, the contribution of Enterococcus species to BA formation in fresh marine fish remains poorly characterized. The present study aimed to isolate and identify Enterococcus spp. from fresh anchovy (Engraulis encrasicolus) and to evaluate their capacity to produce major BAs. A total of 56 fresh anchovy samples were analyzed, yielding 24 Enterococcus isolates that were characterized by phenotypic methods and 16S rRNA gene sequencing. The BA production capacities of the isolates were quantified via HPLC following incubation in a standardized liquid screening medium under optimized laboratory conditions. Fourteen isolates (58.33%) exhibited aminogenic activity and were identified as Enterococcus faecalis (42.86%), E. faecium (28.57%), E. lactis (21.43%), and E. durans (7.14%). Tyramine, histamine, tryptamine, cadaverine, and putrescine were detected, with maximum concentrations reaching 307.638, 257.939, 236.928, 165.835, and 56.317 mg/L, respectively. The highest total BA levels, E. faecium BLK18, exhibited the highest levels, reaching 493.547 mg/L. These findings demonstrate that fresh anchovies may serve as a reservoir for aminogenic Enterococcus spp. and highlight their potential role in BA accumulation beyond traditionally implicated bacteria. The results support the inclusion of Enterococcus species in routine monitoring programs for fresh fish products and underline the need for broader, evidence-based strategies to manage BA-related hazards in seafood.
References
Aktop, S., Şanlıbaba, P. (2026). Isolation and Identification of Biogenic Amines Producer Enterococcus Strains Isolated from Traditional Cheeses. Ital. J. Food Sci., 38 (1): 47–59. https://doi.org/10.15586/ ijfs.v38i1.3302
Al Bulushi, I., Poole, S., Deeth, H. C., Dykes, G. A. (2009). Biogenic amines in fish: roles in intoxication, spoilage, and nitrosamine formation--a review. Crit. Rev. Food Sci. Nutr., 49(4): 369-377. https://doi.org/10.1080/1040839080206751460
Arranz, D., Fernández, E., Szekeres, B., Carvalho, A., Rio, B.D., Redruello, B., Alvarez, M.A. (2025). Tryptamine accumulates in cheese mainly via the decarboxylation of tryptophan by lactic acid bacteria. Food Res. Int., 115380. https://doi.org/10.1016/j.foodres.2024.115380
Arulkumar, A., Paramithiotis, S., Paramasivam, S. (2023). Biogenic amines in fresh fish and fishery products and emerging control. Aquac. Fish., 8(4): 431-450. https://doi.org/10.1016/ j.aaf.2021.02.001
Atasoy, G., Şanlıbaba, P., Vural, N., Anlı, R.E. (2025). Production of Biogenic Amines by Enterococcus Strains from Green and Black Table Olives in Türkiye. Ital. J. Food Sci., 37(3): 310-324. https://doi.org/10.15586/ijfs.v37i3.3043
Ba, H.V., Seo, H.W., Cho, S.H., Kim, Y.S., Kim, J.H., Park, B.Y., Kim, H.W., Ham, J.S., Seong, P.N. (2017). Utilisation possibility of Enterococcus faecalis isolates from neonate's faeces for production of fermented sausages as starter cultures. Int. J. Food Sci. Technol., 52 (7): 1660–1669, https://doi.org/10.1111/ijfs.13440
Banicod, R. J.S., Ntege, W., Njiru, M.N., Abubakar, W. H., Kanthenga, H. T., Javaid, A., Khan, F. (2025). Production and transformation of biogenic amines in different food products by the metabolic activity of the lactic acid bacteria. Int. J. Food Microbiol., 428: 110996, https://doi.org/10.1016/ j.ijfoodmicro.2024.110996
Barbieri, F., Montanari, C., Gardini, F., Tabanelli, G. (2019). Biogenic Amine Production by Lactic Acid Bacteria: A Review. Foods, 8(1): 17. https://doi.org/10.3390/foods8010017
Barbieri, F., Tabanelli, G., Montanari,C., Dall'Osso, N., Šimat, V., Smole Možina, S., Baños,A., Ozogul, F., Bassi, D., Fontana, C., Gardini, F. (2021). Mediterranean spontaneously fermented sausages: Spotlight on microbiological and quality features to exploit their bacterial biodiversity. Foods,10: 2691, https://doi.org/10.3390/foods10112691
Bayesen, D., Yüksel, Z. (2023). Biyojen Aminlerin Fermente Gıdalarda Oluşum Süreci ve Etkileri. İstanbul Rumeli Üniversitesi Sağlık Bilimleri Dergisi, 2(2): 50-65.
Beasley, S. S., Saris, P. E. (2004). Nisin-producing Lactococcus lactis strains isolated from human milk. Appl. Environ. Microbiol., 70(8): 5051-5053. https://doi.org/10.1128/AEM.70.8.5051-5053.2004
Bover-Cid, S., Holzapfel, W. H. (1999). Improved screening procedure for biogenic amine production by lactic acid bacteria. Int. J. Food Microbiol., 53(1): 33-41. https://doi.org/10.1016/S0168-1605(99)00152-X
Buňka, F., Budinský, P., Zimáková, B., Merhaut, M., Flasarová, R., Pachlová, V., Kubáň, V., Buňková, L. (2013). Biogenic amines occurrence in fish meat sampled from restaurants in region of Czech Republic. Food Control, 31 (1): 49-52, https://doi.org/10.1016/j.foodcont.2012.09.044
Çakmak, T., Sancak, Y. C. (2023). Determination of Biogenic Amine Formation, Microbiological and Sensory Changes in Carp (Cyprinus carpio L., 1758) Stored at Cold (4 °C). Van Vet. J., 34(1): 32-42. https://doi.org/10.36483/vanvetj.1209788
Dankar, I., Melhem, A., Serhan, M., Hassan, H.F. (2025). Microbial and processing factors affecting biogenic amine formation and accumulation in dairy: a narrative review. Appl. Food Res., 5(2): 101376, https://doi.org/10.1016/j.afres.2025.101376
Dara, A., Akhondzadeh Basti, A., Mahasti Shotorbani, P., Tamadoni Jahromi, S., Jabar Zadeh Shiadeh, M., Azizian, A. (2025). Investigating histamine levels, microbial and chemical properties in industrial and traditional drying methods of anchovy fish in Qeshm Island. Arch. Razi Inst., 80(1): 131-137. https://doi.org/10.32592/ARI.2025.80.1.131
Del Rio, B., Redruello, B., Linares, D.M., Ladero, V., Fernandez, M., Martin, M.C., Ruas-Madiedo, P., Alvarez, M.A. (2017). The dietary biogenic amines tyramine and histamine show synergistic toxicity towards intestinal cells in culture. Food Chem., 218:249-255. https://doi.org/10.1016/j.foodchem.2016.09.046
Dilireba, E., Lu, Q., Chang, L., Luo, F. (2025). Antibiotic resistance profile and molecular mechanism of enterococci in traditional fermented yogurts. J. Dairy Sci., https://doi.org/10.3168/jds.2025-27212
Ding, T., Li, Y. (2024). Biogenic amines are important indices for characterizing the freshness and hygienic quality of aquatic products: A review. LWT, 194: 115793, https://doi.org/10.1016/j.lwt.2024.115793
EFSA (European Food Safety Authority). (2011). Scientific opinion on risk based control of biogenic amine formation in fermented foods. Panel on Biological Hazards (BIOHAZ). Efsa J., 9(10): 2393-2487. https://doi.org/10.2903/j.efsa.2011.2393
Elkassas, W., Fawzy Elbahy, E. (2016). Determination of Some Biogenic Amines Levels in Some Cheese Varieties. Assiut Vet. Med. J., 62(148), 84-91. https://doi.org/10.21608/avmj.2016.169220
Fadhlaoui-Zid, K., Curiel, J. A., Landeta, G., Fattouch, S., Reverón, I., De Las Rivas, B., Sadok, S., Muñoz, R. (2012). Biogenic amine production by bacteria isolated from ice-preserved sardine and mackerel. Food Control, 25(1): 89-95.
Gao, X., Li, C., He, R., Zhang, Y., Wang, B., Zhang, Z. H., Ho, C. T. (2023). Research advances on biogenic amines in traditional fermented foods: Emphasis on formation mechanism, detection and control methods. Food Chem., 405, Part A,134911. https://doi.org/10.1016/j.foodchem.2022.134911
Ghayoomi, H., Edalatian Dovom, M.R., Habibi Najafi, M.B., Pourfarzad, A. (2024). The principal component analysis of key and significant features of the safety and nutritional value of Mahyaveh sauce. Food Sci. Nutr., 12(4):2896-2907. https://doi.org/10.1002/fsn3.3970
In, J. J., Shim, K. B., Lee, J. B., Bae, Y. J., Kwon, G. Y., Lee, H. R., Park, S., Sohn, S. K. (2024). Effect of activated carbon-based two-stage adsorption on biogenic amine reduction and quality of anchovy fish sauce at industrial scale. Food Chem., 458: 140169. https://doi.org/10.1016/j.foodchem.2024.140169
Javaid, A., Tabassum, N., Karthikeyan, A., Kim, Y.M., Jung, W.K., Khan, F. (2025). Prevalence and stable acquisition of biogenic amine-synthesizing genes in lactic acid bacteria across diverse niches: implications for food safety and human health. NPJ Sci. Food, 9(1): 268. https://doi.org/10.1038/s41538-025-00667-6
Kang, H.R., Kim, H.S., Mah, J.H., Kim, Y.W., Hwang, H.J. (2017). Tyramine reduction by tyrosine decarboxylase inhibitor in Enterococcus faecium for tyramine controlled cheonggukjang. Food Sci. Biotechnol., 27(1):87-93. https://doi.org/10.1007/s10068-017-0205-0
Kočar, D., Köse, S., Tufan, B., Ščavničar, A., Pompe, M. (2021). Determination of Biogenic Amines in Fresh Fish and Processed Fish Products Using IC-MS/MS. Foods, 10(8): 1746. https://doi.org/10.3390/foods10081746
Kukułowicz, A., Steinka, I., Gardocka, M. (2024). Enterococcus spp. in fish: Analysis of the presence and resistance in samples from Tri-City, Poland. PLoS One, 19(7):e0306826. https://doi.org/10.1371/journal.pone.0306826
Ladero, V., Calles-Enríquez, M., Fernández, M., Alvarez, M. A. (2021). Toxicological effects of dietary biogenic amines. Curr. Nutr. Food Sci., 6(2): 145-156. https://doi.org/10.2174/157340110791233256
Li, P., Chen, Y., Bai, J., Yang, H., He, P., Zeng, J. (2025). The Determination of Eight Biogenic Amines Using MSPE-UHPLC-MS/MS and Their Application in Regard to Changes in These Biogenic Amines in Traditional Chinese Dish-Pickled Swimming Crabs. Molecules, 30(6):1353. https://doi.org/10.3390/molecules30061353
Lo Magro, S., Summa, S., Iammarino, M., D’Antini, P., Marchesani, G., Chiaravalle, A.E., Muscarella, M. (2020). A 5-Years (2015–2019) Control Activity of an EU Laboratory: Contamination of Histamine in Fish Products and Exposure Assessment. Appl. Sci., 10: 8693. https://doi.org/10.3390/app10238693
Ma, X., Bi, J., Li, X., Zhang, G., Hao, H., Hou, H. (2021). Contribution of Microorganisms to Biogenic Amine Accumulation during Fish Sauce Fermentation and Screening of Novel Starters. Foods. 10(11):2572. https://doi.org/10.3390/foods10112572
Maddaloni, L., Grasso, S., De Gara, L., Pennazza, G., Zompanti, A., Rapa, M., Ruggieri, R., Vinci, G., Santonico, M. (2021). An electrochemical sensor for monitoring biogenic amines in anchovies as quality and safety index. Sens. Actuators B: Chem., 347, 130648. https://doi.org/10.1016/ j.snb.2021.130648
Maijala, R. L. (1993). Formation of histamine and tyramine by some lactic acid bacteria in MRS‐broth and modified decarboxylation agar. Lett. Appl. Microbiol., 17(1): 40-43. https://doi.org/10.1111/j.1472-765X.1993.tb01431.x
Meng, J., Yang, Q., Wan, W., Zhu, Q., Zeng, X. (2022). Physicochemical properties and adaptability of amine-producing Enterobacteriaceae isolated from traditional Chinese fermented fish (Suan yu). Food Chem., 369: 130885. https://doi.org/10.1016/j.foodchem.2021.130885
Muhtar, A., Jian, P., Muhammad, T., Zhao, J., Dolkun, A., Zhou, T., Piletsky, S. A. (2025). A dummy template molecularly imprinted polymer-coated fiber array extraction for simultaneous HPLC analysis of eight biogenic amines in fermented horse milk. Anal. Chim. Acta. 1352:343901. https://doi.org/10.1016/j.aca.2025.343901
Mutalipassi, M., D’Anza, E., Pugliano, M., Firmamento, R., Murano, C., Ruocco, N., Pennesi, C., Procaccini, G., Romeo, T., Terlizzi, A., Peretti, V. (2024). Casting light on the European anchovy: from biology to conservation and industry. Front. Ecol. Evol., 12: 1352055. https://doi.org/10.3389 /fevo.2024.1352055
Ozogul, F., Durmuş, M., Kosker, A.R., Özkütük, A.S., Kuley, E., Yazgan, H., Yazgan, R., Simat, V., Ozogul, Y. (2023). The impact of marine and terrestrial based extracts on the freshness quality of modified atmosphere packed sea bass fillets. Food Biosci., 53:102545. https://doi.org/10.1016/j.fbio.2023.102545
Özyurt, G., Özkütük, A. S., Boğa, E. K. (2022). Türk Marketlerinde Satışa Sunulan Çeşitli Balık Ürünlerinin Biyojenik Amin ve Trimetilamin İçerikleri. Act. Aqua. Tr., 18(1): 13-23. https://doi.org/10.22392/actaquatr.906996
Park, Y. K., Jin, Y. H., Lee, J.-H., Byun, B. Y., Lee, J., Jeong, K. C., Mah, J.-H. (2020). The Role of Enterococcus faecium as a Key Producer and Fermentation Condition as an Influencing Factor in Tyramine Accumulation in Cheonggukjang. Foods, 9(7), 915. https://doi.org/10.3390/foods9070915
Pawul-Gruba, M., Denis, E., Kiljanek, T., Osek, J. (2025). Prevalence of Biogenic Amines and Their Relation to the Bacterial Content in Ripened Cheeses on the Retail Market in Poland. Foods, 14: 2478. https://doi.org/10.3390/foods14142478
Pertiwi, R.M., Nurilmala, M., Abdullah, A., Nurjanah, Yusfiandayani, R., Sondita, M.F.A. (2020). Deteksi bakteri pembentuk amina biogenik pada ikan Scombridae secara multiplex PCR. J. Pengolah. Has. Perik. Indones., 23(2): 359-371.
Pons-Sánchez-Cascado, S., Bover-Cid, S., Veciana-Nogués, M. T., Vidal-Carou, M. C. (2005). Amino acid-decarboxylase activity of bacteria isolated from ice-preserved anchovies. Eur. Food Res. Technol., 220: 312–315. https://doi.org/10.1007/s00217-004-1095-y
Ruiz-Capillas, C., Herrero, A. M. (2019). Impact of Biogenic Amines on Food Quality and Safety. Foods, 8(2):62. https://doi.org/10.3390/foods8020062
Sadighara, P., Bekheir, S.A., Shafaroodi, H., Basaran, B., Sadighara, M. (2024). Tyramine, a biogenic agent in cheese: amount and factors affecting its formation, a systematic review. Food Prod. Process and Nutr., 6:30. https://doi.org/10.1186/s43014-024-00223-x
Sánchez-Pérez, S., Comas-Basté, O., Costa-Catala, J., Iduriaga-Platero, I., Veciana-Nogués, M.T., Vidal-Carou, M.C., Latorre-Moratalla, M.L. (2022). The Rate of Histamine Degradation by Diamine Oxidase Is Compromised by Other Biogenic Amines. Front. Nutr., 9:897028. https://doi.org/10.3389/fnut.2022.897028
Sang, X., Li, K., Zhu, Y., Ma, X., Hao, H., Bi, J., Hou, H. (2020). The impact of microbial diversity on biogenic amines formation in grasshopper sub shrimp paste during the fermentation. Front. Microbiol. 11: 782. https://doi.org/10.3389/fmicb.2020.00782
Shanab, O., Fareed, F., Nassar, A.Y., Abd-Elhafeez, H.H., Ahmed, A.S., El-Zamkan, M. (2025). Molecular characterization of histidine and tyrosine decarboxylating Enterococcus species isolated from some milk products. BMC Microbiol., 25, 234. https://doi.org/10.1186/s12866-025-03940-6
Tabanelli, G. (2020). Biogenic Amines and Food Quality: Emerging Challenges and Public Health Concerns. Foods, 9: 859. https://doi.org/10.3390/foods9070859
Ucar, Y., Ozogul, F. (2024). Biogenic Amines in Seafood. Food Bull., 3(1): 9-15. https://doi.org/10.61326/foodb.v3i1.258
Visciano, P., Schirone, M., Tofalo, R., Suzzi, G. (2012). Biogenic Amines in Raw and Processed Seafood. Front. Microbiol., 3: 188, https://doi.org/10.3389/fmicb.2012.00188
Visciano, P., Schirone, M., Paparella, A. (2020). An Overview of Histamine and Other Biogenic Amines in Fish and Fish Products. Foods, 9(12): 1795. https://doi.org/10.3390/foods9121795
Wiśniewski, P., Barbieri, F. (2025). Molecular Identification and Biogenic Amine Production Capacity of Enterococcus faecalis Strains Isolated from Raw Milk. Int. J. Mol. Sci., 26(21): 10480. https://doi.org/10.3390/ijms262110480
Yilmaz N. (2024). Quantitative analysis of biogenic amine production of different lactic acid bacteria isolated from ready-to-eat packaged fish products. Vet. Res. Forum. 15(10):537-543. https://doi.org/10.30466/vrf.2024.2024103.4193
Zeng, X., Xia, W., Yang, F., Jiang, Q. (2013). Changes of biogenic amines in Chinese low-salt fermented fish pieces (Suan yu) inoculated with mixed starter cultures, Int. J. Food Sci. Technol., 48 (4): 685–692, https://doi.org/10.1111/ijfs.12010
Zhang, X., Chi, H., Peng, D., Jiang, M., Wang, C., Zhang, H., Kang, W., Li, L. (2025). Integrated Metagenomic and LC–MS/MS Analysis Reveals the Biogenic Amine-Producing Strains of Two Typical Chinese Traditional Fish Products: Fermented Mandarin Fish (Siniperca chuatsi) and Semi-Dried Yellow Croaker (Larimichthys crocea). Foods, 14(6): 1016. https://doi.org/10.3390/foods14061016
Zhernov, Y. V., Simanduyev, M. Y., Zaostrovtseva, O. K., Semeniako, E. E., Kolykhalova, K. I., Fadeeva, I. A., Kashutina, M. I., Vysochanskaya, S. O., Belova, E. V., Shcherbakov, D. V., Sukhov, V. A., Sidorova, E. A., Mitrokhin, O. V. (2023). Molecular Mechanisms of Scombroid Food Poisoning. Int. J. Mol. Sci., 24(1): 809. https://doi.org/10.3390/ijms24010809
Al Bulushi, I., Poole, S., Deeth, H. C., Dykes, G. A. (2009). Biogenic amines in fish: roles in intoxication, spoilage, and nitrosamine formation--a review. Crit. Rev. Food Sci. Nutr., 49(4): 369-377. https://doi.org/10.1080/1040839080206751460
Arranz, D., Fernández, E., Szekeres, B., Carvalho, A., Rio, B.D., Redruello, B., Alvarez, M.A. (2025). Tryptamine accumulates in cheese mainly via the decarboxylation of tryptophan by lactic acid bacteria. Food Res. Int., 115380. https://doi.org/10.1016/j.foodres.2024.115380
Arulkumar, A., Paramithiotis, S., Paramasivam, S. (2023). Biogenic amines in fresh fish and fishery products and emerging control. Aquac. Fish., 8(4): 431-450. https://doi.org/10.1016/ j.aaf.2021.02.001
Atasoy, G., Şanlıbaba, P., Vural, N., Anlı, R.E. (2025). Production of Biogenic Amines by Enterococcus Strains from Green and Black Table Olives in Türkiye. Ital. J. Food Sci., 37(3): 310-324. https://doi.org/10.15586/ijfs.v37i3.3043
Ba, H.V., Seo, H.W., Cho, S.H., Kim, Y.S., Kim, J.H., Park, B.Y., Kim, H.W., Ham, J.S., Seong, P.N. (2017). Utilisation possibility of Enterococcus faecalis isolates from neonate's faeces for production of fermented sausages as starter cultures. Int. J. Food Sci. Technol., 52 (7): 1660–1669, https://doi.org/10.1111/ijfs.13440
Banicod, R. J.S., Ntege, W., Njiru, M.N., Abubakar, W. H., Kanthenga, H. T., Javaid, A., Khan, F. (2025). Production and transformation of biogenic amines in different food products by the metabolic activity of the lactic acid bacteria. Int. J. Food Microbiol., 428: 110996, https://doi.org/10.1016/ j.ijfoodmicro.2024.110996
Barbieri, F., Montanari, C., Gardini, F., Tabanelli, G. (2019). Biogenic Amine Production by Lactic Acid Bacteria: A Review. Foods, 8(1): 17. https://doi.org/10.3390/foods8010017
Barbieri, F., Tabanelli, G., Montanari,C., Dall'Osso, N., Šimat, V., Smole Možina, S., Baños,A., Ozogul, F., Bassi, D., Fontana, C., Gardini, F. (2021). Mediterranean spontaneously fermented sausages: Spotlight on microbiological and quality features to exploit their bacterial biodiversity. Foods,10: 2691, https://doi.org/10.3390/foods10112691
Bayesen, D., Yüksel, Z. (2023). Biyojen Aminlerin Fermente Gıdalarda Oluşum Süreci ve Etkileri. İstanbul Rumeli Üniversitesi Sağlık Bilimleri Dergisi, 2(2): 50-65.
Beasley, S. S., Saris, P. E. (2004). Nisin-producing Lactococcus lactis strains isolated from human milk. Appl. Environ. Microbiol., 70(8): 5051-5053. https://doi.org/10.1128/AEM.70.8.5051-5053.2004
Bover-Cid, S., Holzapfel, W. H. (1999). Improved screening procedure for biogenic amine production by lactic acid bacteria. Int. J. Food Microbiol., 53(1): 33-41. https://doi.org/10.1016/S0168-1605(99)00152-X
Buňka, F., Budinský, P., Zimáková, B., Merhaut, M., Flasarová, R., Pachlová, V., Kubáň, V., Buňková, L. (2013). Biogenic amines occurrence in fish meat sampled from restaurants in region of Czech Republic. Food Control, 31 (1): 49-52, https://doi.org/10.1016/j.foodcont.2012.09.044
Çakmak, T., Sancak, Y. C. (2023). Determination of Biogenic Amine Formation, Microbiological and Sensory Changes in Carp (Cyprinus carpio L., 1758) Stored at Cold (4 °C). Van Vet. J., 34(1): 32-42. https://doi.org/10.36483/vanvetj.1209788
Dankar, I., Melhem, A., Serhan, M., Hassan, H.F. (2025). Microbial and processing factors affecting biogenic amine formation and accumulation in dairy: a narrative review. Appl. Food Res., 5(2): 101376, https://doi.org/10.1016/j.afres.2025.101376
Dara, A., Akhondzadeh Basti, A., Mahasti Shotorbani, P., Tamadoni Jahromi, S., Jabar Zadeh Shiadeh, M., Azizian, A. (2025). Investigating histamine levels, microbial and chemical properties in industrial and traditional drying methods of anchovy fish in Qeshm Island. Arch. Razi Inst., 80(1): 131-137. https://doi.org/10.32592/ARI.2025.80.1.131
Del Rio, B., Redruello, B., Linares, D.M., Ladero, V., Fernandez, M., Martin, M.C., Ruas-Madiedo, P., Alvarez, M.A. (2017). The dietary biogenic amines tyramine and histamine show synergistic toxicity towards intestinal cells in culture. Food Chem., 218:249-255. https://doi.org/10.1016/j.foodchem.2016.09.046
Dilireba, E., Lu, Q., Chang, L., Luo, F. (2025). Antibiotic resistance profile and molecular mechanism of enterococci in traditional fermented yogurts. J. Dairy Sci., https://doi.org/10.3168/jds.2025-27212
Ding, T., Li, Y. (2024). Biogenic amines are important indices for characterizing the freshness and hygienic quality of aquatic products: A review. LWT, 194: 115793, https://doi.org/10.1016/j.lwt.2024.115793
EFSA (European Food Safety Authority). (2011). Scientific opinion on risk based control of biogenic amine formation in fermented foods. Panel on Biological Hazards (BIOHAZ). Efsa J., 9(10): 2393-2487. https://doi.org/10.2903/j.efsa.2011.2393
Elkassas, W., Fawzy Elbahy, E. (2016). Determination of Some Biogenic Amines Levels in Some Cheese Varieties. Assiut Vet. Med. J., 62(148), 84-91. https://doi.org/10.21608/avmj.2016.169220
Fadhlaoui-Zid, K., Curiel, J. A., Landeta, G., Fattouch, S., Reverón, I., De Las Rivas, B., Sadok, S., Muñoz, R. (2012). Biogenic amine production by bacteria isolated from ice-preserved sardine and mackerel. Food Control, 25(1): 89-95.
Gao, X., Li, C., He, R., Zhang, Y., Wang, B., Zhang, Z. H., Ho, C. T. (2023). Research advances on biogenic amines in traditional fermented foods: Emphasis on formation mechanism, detection and control methods. Food Chem., 405, Part A,134911. https://doi.org/10.1016/j.foodchem.2022.134911
Ghayoomi, H., Edalatian Dovom, M.R., Habibi Najafi, M.B., Pourfarzad, A. (2024). The principal component analysis of key and significant features of the safety and nutritional value of Mahyaveh sauce. Food Sci. Nutr., 12(4):2896-2907. https://doi.org/10.1002/fsn3.3970
In, J. J., Shim, K. B., Lee, J. B., Bae, Y. J., Kwon, G. Y., Lee, H. R., Park, S., Sohn, S. K. (2024). Effect of activated carbon-based two-stage adsorption on biogenic amine reduction and quality of anchovy fish sauce at industrial scale. Food Chem., 458: 140169. https://doi.org/10.1016/j.foodchem.2024.140169
Javaid, A., Tabassum, N., Karthikeyan, A., Kim, Y.M., Jung, W.K., Khan, F. (2025). Prevalence and stable acquisition of biogenic amine-synthesizing genes in lactic acid bacteria across diverse niches: implications for food safety and human health. NPJ Sci. Food, 9(1): 268. https://doi.org/10.1038/s41538-025-00667-6
Kang, H.R., Kim, H.S., Mah, J.H., Kim, Y.W., Hwang, H.J. (2017). Tyramine reduction by tyrosine decarboxylase inhibitor in Enterococcus faecium for tyramine controlled cheonggukjang. Food Sci. Biotechnol., 27(1):87-93. https://doi.org/10.1007/s10068-017-0205-0
Kočar, D., Köse, S., Tufan, B., Ščavničar, A., Pompe, M. (2021). Determination of Biogenic Amines in Fresh Fish and Processed Fish Products Using IC-MS/MS. Foods, 10(8): 1746. https://doi.org/10.3390/foods10081746
Kukułowicz, A., Steinka, I., Gardocka, M. (2024). Enterococcus spp. in fish: Analysis of the presence and resistance in samples from Tri-City, Poland. PLoS One, 19(7):e0306826. https://doi.org/10.1371/journal.pone.0306826
Ladero, V., Calles-Enríquez, M., Fernández, M., Alvarez, M. A. (2021). Toxicological effects of dietary biogenic amines. Curr. Nutr. Food Sci., 6(2): 145-156. https://doi.org/10.2174/157340110791233256
Li, P., Chen, Y., Bai, J., Yang, H., He, P., Zeng, J. (2025). The Determination of Eight Biogenic Amines Using MSPE-UHPLC-MS/MS and Their Application in Regard to Changes in These Biogenic Amines in Traditional Chinese Dish-Pickled Swimming Crabs. Molecules, 30(6):1353. https://doi.org/10.3390/molecules30061353
Lo Magro, S., Summa, S., Iammarino, M., D’Antini, P., Marchesani, G., Chiaravalle, A.E., Muscarella, M. (2020). A 5-Years (2015–2019) Control Activity of an EU Laboratory: Contamination of Histamine in Fish Products and Exposure Assessment. Appl. Sci., 10: 8693. https://doi.org/10.3390/app10238693
Ma, X., Bi, J., Li, X., Zhang, G., Hao, H., Hou, H. (2021). Contribution of Microorganisms to Biogenic Amine Accumulation during Fish Sauce Fermentation and Screening of Novel Starters. Foods. 10(11):2572. https://doi.org/10.3390/foods10112572
Maddaloni, L., Grasso, S., De Gara, L., Pennazza, G., Zompanti, A., Rapa, M., Ruggieri, R., Vinci, G., Santonico, M. (2021). An electrochemical sensor for monitoring biogenic amines in anchovies as quality and safety index. Sens. Actuators B: Chem., 347, 130648. https://doi.org/10.1016/ j.snb.2021.130648
Maijala, R. L. (1993). Formation of histamine and tyramine by some lactic acid bacteria in MRS‐broth and modified decarboxylation agar. Lett. Appl. Microbiol., 17(1): 40-43. https://doi.org/10.1111/j.1472-765X.1993.tb01431.x
Meng, J., Yang, Q., Wan, W., Zhu, Q., Zeng, X. (2022). Physicochemical properties and adaptability of amine-producing Enterobacteriaceae isolated from traditional Chinese fermented fish (Suan yu). Food Chem., 369: 130885. https://doi.org/10.1016/j.foodchem.2021.130885
Muhtar, A., Jian, P., Muhammad, T., Zhao, J., Dolkun, A., Zhou, T., Piletsky, S. A. (2025). A dummy template molecularly imprinted polymer-coated fiber array extraction for simultaneous HPLC analysis of eight biogenic amines in fermented horse milk. Anal. Chim. Acta. 1352:343901. https://doi.org/10.1016/j.aca.2025.343901
Mutalipassi, M., D’Anza, E., Pugliano, M., Firmamento, R., Murano, C., Ruocco, N., Pennesi, C., Procaccini, G., Romeo, T., Terlizzi, A., Peretti, V. (2024). Casting light on the European anchovy: from biology to conservation and industry. Front. Ecol. Evol., 12: 1352055. https://doi.org/10.3389 /fevo.2024.1352055
Ozogul, F., Durmuş, M., Kosker, A.R., Özkütük, A.S., Kuley, E., Yazgan, H., Yazgan, R., Simat, V., Ozogul, Y. (2023). The impact of marine and terrestrial based extracts on the freshness quality of modified atmosphere packed sea bass fillets. Food Biosci., 53:102545. https://doi.org/10.1016/j.fbio.2023.102545
Özyurt, G., Özkütük, A. S., Boğa, E. K. (2022). Türk Marketlerinde Satışa Sunulan Çeşitli Balık Ürünlerinin Biyojenik Amin ve Trimetilamin İçerikleri. Act. Aqua. Tr., 18(1): 13-23. https://doi.org/10.22392/actaquatr.906996
Park, Y. K., Jin, Y. H., Lee, J.-H., Byun, B. Y., Lee, J., Jeong, K. C., Mah, J.-H. (2020). The Role of Enterococcus faecium as a Key Producer and Fermentation Condition as an Influencing Factor in Tyramine Accumulation in Cheonggukjang. Foods, 9(7), 915. https://doi.org/10.3390/foods9070915
Pawul-Gruba, M., Denis, E., Kiljanek, T., Osek, J. (2025). Prevalence of Biogenic Amines and Their Relation to the Bacterial Content in Ripened Cheeses on the Retail Market in Poland. Foods, 14: 2478. https://doi.org/10.3390/foods14142478
Pertiwi, R.M., Nurilmala, M., Abdullah, A., Nurjanah, Yusfiandayani, R., Sondita, M.F.A. (2020). Deteksi bakteri pembentuk amina biogenik pada ikan Scombridae secara multiplex PCR. J. Pengolah. Has. Perik. Indones., 23(2): 359-371.
Pons-Sánchez-Cascado, S., Bover-Cid, S., Veciana-Nogués, M. T., Vidal-Carou, M. C. (2005). Amino acid-decarboxylase activity of bacteria isolated from ice-preserved anchovies. Eur. Food Res. Technol., 220: 312–315. https://doi.org/10.1007/s00217-004-1095-y
Ruiz-Capillas, C., Herrero, A. M. (2019). Impact of Biogenic Amines on Food Quality and Safety. Foods, 8(2):62. https://doi.org/10.3390/foods8020062
Sadighara, P., Bekheir, S.A., Shafaroodi, H., Basaran, B., Sadighara, M. (2024). Tyramine, a biogenic agent in cheese: amount and factors affecting its formation, a systematic review. Food Prod. Process and Nutr., 6:30. https://doi.org/10.1186/s43014-024-00223-x
Sánchez-Pérez, S., Comas-Basté, O., Costa-Catala, J., Iduriaga-Platero, I., Veciana-Nogués, M.T., Vidal-Carou, M.C., Latorre-Moratalla, M.L. (2022). The Rate of Histamine Degradation by Diamine Oxidase Is Compromised by Other Biogenic Amines. Front. Nutr., 9:897028. https://doi.org/10.3389/fnut.2022.897028
Sang, X., Li, K., Zhu, Y., Ma, X., Hao, H., Bi, J., Hou, H. (2020). The impact of microbial diversity on biogenic amines formation in grasshopper sub shrimp paste during the fermentation. Front. Microbiol. 11: 782. https://doi.org/10.3389/fmicb.2020.00782
Shanab, O., Fareed, F., Nassar, A.Y., Abd-Elhafeez, H.H., Ahmed, A.S., El-Zamkan, M. (2025). Molecular characterization of histidine and tyrosine decarboxylating Enterococcus species isolated from some milk products. BMC Microbiol., 25, 234. https://doi.org/10.1186/s12866-025-03940-6
Tabanelli, G. (2020). Biogenic Amines and Food Quality: Emerging Challenges and Public Health Concerns. Foods, 9: 859. https://doi.org/10.3390/foods9070859
Ucar, Y., Ozogul, F. (2024). Biogenic Amines in Seafood. Food Bull., 3(1): 9-15. https://doi.org/10.61326/foodb.v3i1.258
Visciano, P., Schirone, M., Tofalo, R., Suzzi, G. (2012). Biogenic Amines in Raw and Processed Seafood. Front. Microbiol., 3: 188, https://doi.org/10.3389/fmicb.2012.00188
Visciano, P., Schirone, M., Paparella, A. (2020). An Overview of Histamine and Other Biogenic Amines in Fish and Fish Products. Foods, 9(12): 1795. https://doi.org/10.3390/foods9121795
Wiśniewski, P., Barbieri, F. (2025). Molecular Identification and Biogenic Amine Production Capacity of Enterococcus faecalis Strains Isolated from Raw Milk. Int. J. Mol. Sci., 26(21): 10480. https://doi.org/10.3390/ijms262110480
Yilmaz N. (2024). Quantitative analysis of biogenic amine production of different lactic acid bacteria isolated from ready-to-eat packaged fish products. Vet. Res. Forum. 15(10):537-543. https://doi.org/10.30466/vrf.2024.2024103.4193
Zeng, X., Xia, W., Yang, F., Jiang, Q. (2013). Changes of biogenic amines in Chinese low-salt fermented fish pieces (Suan yu) inoculated with mixed starter cultures, Int. J. Food Sci. Technol., 48 (4): 685–692, https://doi.org/10.1111/ijfs.12010
Zhang, X., Chi, H., Peng, D., Jiang, M., Wang, C., Zhang, H., Kang, W., Li, L. (2025). Integrated Metagenomic and LC–MS/MS Analysis Reveals the Biogenic Amine-Producing Strains of Two Typical Chinese Traditional Fish Products: Fermented Mandarin Fish (Siniperca chuatsi) and Semi-Dried Yellow Croaker (Larimichthys crocea). Foods, 14(6): 1016. https://doi.org/10.3390/foods14061016
Zhernov, Y. V., Simanduyev, M. Y., Zaostrovtseva, O. K., Semeniako, E. E., Kolykhalova, K. I., Fadeeva, I. A., Kashutina, M. I., Vysochanskaya, S. O., Belova, E. V., Shcherbakov, D. V., Sukhov, V. A., Sidorova, E. A., Mitrokhin, O. V. (2023). Molecular Mechanisms of Scombroid Food Poisoning. Int. J. Mol. Sci., 24(1): 809. https://doi.org/10.3390/ijms24010809
Article Sidebar
Published
May 14, 2026
Article Details
How to Cite
Ergezen, G. ., Atasoy, G., Şanlıbaba, P., Vural, N., & Anlı, R. E. . (2026). Biogenic amine–producing Enterococcus spp. from anchovy (Engraulis encrasicolus): Isolation and molecular insights. Italian Journal of Food Science, 38(2), 214–228. https://doi.org/10.15586/ijfs.v38i2.3563
Section
Original Article
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
Copyright Agreement with Authors
Before publication, after the acceptance of the manuscript, Authors have to sign a Publication Agreement with "Italian Journal of Food Science", granting and assigning to "Italian Journal of Food Science" the perpetual right to distribute the work free of charge by any means and in any parts of the world, including the communication to the public through the journal website.
License for Published Contents
http://creativecommons.org/licenses/by-nc-nd/4.0/
How to Cite
Ergezen, G. ., Atasoy, G., Şanlıbaba, P., Vural, N., & Anlı, R. E. . (2026). Biogenic amine–producing Enterococcus spp. from anchovy (Engraulis encrasicolus): Isolation and molecular insights. Italian Journal of Food Science, 38(2), 214–228. https://doi.org/10.15586/ijfs.v38i2.3563